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Microb Ecol. 2019 Oct;78(3):618-630. doi: 10.1007/s00248-019-01316-8. Epub 2019 Feb 13.

Enhanced Growth of Pilin-Deficient Geobacter sulfurreducens Mutants in Carbon Poor and Electron Donor Limiting Conditions.

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Department of Physiology, Anatomy and Microbiology, La Trobe University, Melbourne, Victoria, Australia.
Bioinformatics and Cancer Genomics, Research Division, Peter MacCallum Cancer Centre, Melbourne, Victoria, Australia.
Advanced Water Management Centre, The University of Queensland, Brisbane, Queensland, Australia.
Department of Physiology, Anatomy and Microbiology, La Trobe University, Melbourne, Victoria, Australia.
Centre for Future Landscapes, La Trobe University, Melbourne, Australia.


Geobacter sulfurreducens pili enable extracellular electron transfer and play a role in secretion of c-type cytochromes such as OmcZ. PilA-deficient mutants of G. sulfurreducens have previously been shown to accumulate cytochromes within their membranes. This cytochrome retaining phenotype allowed for enhanced growth of PilA-deficient mutants in electron donor and carbon-limited conditions where formate and fumarate are provided as the sole electron donor and acceptor with no supplementary carbon source. Conversely, wild-type G. sulfurreducens, which has normal secretion of cytochromes, has comparative limited growth in these conditions. This growth is further impeded for OmcZ-deficient and OmcS-deficient mutants. A PilB-deficient mutant which prevents pilin production but allows for secretion of OmcZ had moderate growth in these conditions, indicating a role for cytochrome localization to enabling survival in the electron donor and carbon-limited conditions. To determine which pathways enhanced growth using formate, Sequential Window Acquisition of all Theoretical Mass Spectra mass spectrometry (SWATH-MS) proteomics of formate adapted PilA-deficient mutants and acetate grown wild type was performed. PilA-deficient mutants had an overall decrease in tricarboxylic acid (TCA) cycle enzymes and significant upregulation of electron transport chain associated proteins including many c-type cytochromes and [NiFe]-hydrogenases. Whole genome sequencing of the mutants shows strong convergent evolution and emergence of genetic subpopulations during adaptation to growth on formate. The results described here suggest a role for membrane constrained c-type cytochromes to the enhancement of survival and growth in electron donor and carbon-limited conditions.


Adaptive evolution; Formate; Geobacter sulfurreducens; SWATH-MS proteomics; Whole genome sequencing


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